399
Views
7
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Graphdiyne Oxide-Mediated Photodynamic Therapy Boosts Enhancive T-Cell Immune Responses by Increasing Cellular Stiffness

, , ORCID Icon, , ORCID Icon, , , , & show all
Pages 797-812 | Received 18 Oct 2022, Accepted 14 Jan 2023, Published online: 15 Feb 2023

References

  • Ren ZH, Hu CY, He HR, Li YJ, Lyu J. Global and regional burdens of oral cancer from 1990 to 2017: results from the global burden of disease study. Cancer Commun. 2020;40(2–3):81–92. doi:10.1002/cac2.12009
  • Duan X, He C, Kron SJ, Lin W. Nanoparticle formulations of cisplatin for cancer therapy. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2016;8(5):776–791. doi:10.1002/wnan.1390
  • Boztepe T, Castro GR, Leon IE. Lipid, polymeric, inorganic-based drug delivery applications for platinum-based anticancer drugs. Int J Pharmaceut. 2021;605. doi:10.1016/j.ijpharm.2021.120788
  • Goldberg M, Manzi A, Conway P, et al. A nanoengineered topical transmucosal cisplatin delivery system induces anti-tumor response in animal models and patients with oral cancer. Nat Commun. 2022;13(1):4829. doi:10.1038/s41467-022-31859-3
  • Yamana K, Inoue J, Yoshida R, et al. Extracellular vesicles derived from radioresistant oral squamous cell carcinoma cells contribute to the acquisition of radioresistance via the miR-503-3p-BAK axis. J Extracell Vesicles. 2021;10(14):e12169. doi:10.1002/jev2.12169
  • Karan D, Holzbeierlein JM, Van Veldhuizen P, Thrasher JB. Cancer immunotherapy: a paradigm shift for prostate cancer treatment. Nat Rev Urol. 2012;9(7):376–385. doi:10.1038/nrurol.2012.106
  • Pauken KE, Dougan M, Rose NR, Lichtman AH, Sharpe AH. Adverse events following cancer immunotherapy: obstacles and opportunities. Trends Immunol. 2019;40(6):511–523. doi:10.1016/j.it.2019.04.002
  • Yu WQ, Sun JL, Wang XY, et al. Boosting cancer immunotherapy via the convenient A2AR inhibition using a tunable nanocatalyst with light-enhanced activity. Adv Mater. 2022;34:8. doi:10.1002/adma.202106967
  • Ribas A, Wolchok JD. Cancer immunotherapy using checkpoint blockade. Science. 2018;359(6382):1350. doi:10.1126/science.aar4060
  • Li G, Jiang Y, Qin Y, Yuan S, Chen X. Comparing development strategies for PD1/PDL1-based immunotherapies. Nat Rev Drug Discov. 2022;21(7):484. doi:10.1038/d41573-022-00003-7
  • Dolladille C, Ederhy S, Sassier M, et al. Immune checkpoint inhibitor rechallenge after immune-related adverse events in patients with cancer. JAMA Oncol. 2020;6(6):865–871. doi:10.1001/jamaoncol.2020.0726
  • Eil R, Vodnala SK, Clever D, et al. Ionic immune suppression within the tumour microenvironment limits T cell effector function. Nature. 2016;537(7621):539. doi:10.1038/nature19364
  • Andre P, Denis C, Soulas C, et al. Anti-NKG2A mAb is a checkpoint inhibitor that promotes anti-tumor immunity by unleashing both T and NK cells. Cell. 2018;175(7):1731. doi:10.1016/j.cell.2018.10.014
  • Alibert C, Goud B, Manneville JB. Are cancer cells really softer than normal cells?. Biol Cell. 2017;109(5):167–189. doi:10.1111/boc.201600078
  • Lv J, Liu Y, Cheng F, et al. Cell softness regulates tumorigenicity and stemness of cancer cells. EMBO J. 2021;40(2):e106123. doi:10.15252/embj.2020106123
  • Qin Y, Chen K, Gu W, et al. Small size fullerenol nanoparticles suppress lung metastasis of breast cancer cell by disrupting actin dynamics. J Nanobiotechnology. 2018;16(1):54. doi:10.1186/s12951-018-0380-z
  • Xu WW, Mezencev R, Kim B, Wang LJ, McDonald J, Sulchek T. Cell stiffness is a biomarker of the metastatic potential of ovarian cancer cells. PLoS One. 2012;7:10. doi:10.1371/journal.pone.0046609
  • Usmani SM, Mempel TR. Cancer cells relax and resist cytotoxic attack. Immunity. 2021;54(5):853–855. doi:10.1016/j.immuni.2021.04.017
  • Xie JL, Wang YW, Choi W, et al. Overcoming barriers in photodynamic therapy harnessing nano-formulation strategies. Chem Soc Rev. 2021;50(16):9152–9201. doi:10.1039/d0cs01370f
  • Xiao X, Liang S, Zhao YJ, et al. Multifunctional carbon monoxide nanogenerator as immunogenic cell death drugs with enhanced antitumor immunity and antimetastatic effect. Biomaterials. 2021:277. doi:10.1016/j.biomaterials.2021.121120
  • Hu X, Hou B, Xu Z, et al. Supramolecular prodrug nanovectors for active tumor targeting and combination immunotherapy of colorectal cancer. Adv Sci. 2020;7(8):1903332. doi:10.1002/advs.201903332
  • Fang Y, Liu YX, Qi L, Xue YR, Li YL. 2D graphdiyne: an emerging carbon material. Chem Soc Rev. 2022;51(7):2681–2709. doi:10.1039/d1cs00592h
  • Huang CS, Li YJ, Wang N, et al. Progress in research into 2D graphdiyne-based materials. Chem Rev. 2018;118(16):7744–7803. doi:10.1021/acs.chemrev.8b00288
  • Wang Q, Liu Y, Wang H, et al. Graphdiyne oxide nanosheets display selective anti-leukemia efficacy against DNMT3A-mutant AML cells. Nat Commun. 2022;13(1):5657. doi:10.1038/s41467-022-33410-w
  • Xie ZJ, Peng MH, Lu RT, et al. Black phosphorus-based photothermal therapy with aCD47-mediated immune checkpoint blockade for enhanced cancer immunotherapy. Light Sci Appl. 2020;9:1. doi:10.1038/s41377-020-00388-3
  • Yin F, Hu K, Chen S, et al. Black phosphorus quantum dot based novel siRNA delivery systems in human pluripotent teratoma PA-1 cells. J Mater Chem B. 2017;5(27):5433–5440. doi:10.1039/c7tb01068k
  • Xie ZJ, Chen SY, Duo YH, et al. Biocompatible two-dimensional titanium nanosheets for multimodal imaging-guided cancer theranostics. Acs Appl Mater Inter. 2019;11(25):22129–22140. doi:10.1021/acsami.9b04628
  • Xing CY, Chen SY, Liang X, et al. Two-dimensional MXene (Ti3C2)-Integrated cellulose hydrogels: toward smart three-dimensional network nanoplatforms exhibiting light-induced swelling and bimodal photothermal/chemotherapy anticancer activity. Acs Appl Mater Inter. 2018;10(33):27631–27643. doi:10.1021/acsami.8b08314
  • Xing CY, Chen SY, Qiu M, et al. Conceptually novel black phosphorus/cellulose hydrogels as promising photothermal agents for effective cancer therapy. Adv Healthc Mater. 2018;7(7). doi:10.1002/adhm.201701510
  • Jiang W, Zhang Z, Wang Q, et al. Tumor reoxygenation and blood perfusion enhanced photodynamic therapy using ultrathin graphdiyne oxide nanosheets. Nano Lett. 2019;19(6):4060–4067. doi:10.1021/acs.nanolett.9b01458
  • Xing EY, Du YY, Yin JJ, et al. Multi-functional nanodrug based on a three-dimensional framework for targeted photo-chemo synergetic cancer therapy. Adv Healthc Mater. 2021;10:8. doi:10.1002/adhm.202001874
  • Guo M, Zhao L, Liu J, et al. The underlying function and structural organization of the intracellular protein corona on graphdiyne oxide nanosheet for local immunomodulation. Nano Lett. 2021;21(14):6005–6013. doi:10.1021/acs.nanolett.1c01048
  • Peng G, Duan T, Guo M, et al. Biodegradation of graphdiyne oxide in classically activated (M1) macrophages modulates cytokine production. Nanoscale. 2021;13(30):13072–13084. doi:10.1039/d1nr02473f
  • Zhang D, Feng F, Li Q, Wang X, Yao L. Nanopurpurin-based photodynamic therapy destructs extracellular matrix against intractable tumor metastasis. Biomaterials. 2018;173:22–33. doi:10.1016/j.biomaterials.2018.04.045
  • Liu T, Wu LY, Berkman CE. Prostate-specific membrane antigen-targeted photodynamic therapy induces rapid cytoskeletal disruption. Cancer Lett. 2010;296(1):106–112. doi:10.1016/j.canlet.2010.04.003
  • Yan H, Guo S, Wu F, et al. Carbon atom hybridization matters: ultrafast humidity response of graphdiyne oxides. Angew Chem Int Ed Engl. 2018;57(15):3922–3926. doi:10.1002/anie.201709417
  • Xing E, Du Y, Yin J, et al. Multi-functional nanodrug based on a three-dimensional framework for targeted photo-chemo synergetic cancer therapy. Adv Healthc Mater. 2021;10(8):e2001874. doi:10.1002/adhm.202001874
  • Ma W, Xue Y, Guo S, et al. Graphdiyne oxide: a new carbon nanozyme. Chem Commun. 2020;56(38):5115–5118. doi:10.1039/d0cc01840f
  • Wang YW, Qiu M, Won M, et al. Emerging 2D material-based nanocarrier for cancer therapy beyond graphene. Coordin Chem Rev. 2019:400. doi:10.1016/j.ccr.2019.213041
  • Zhu Y, Xie ZJ, Li JF, et al. From phosphorus to phosphorene: applications in disease theranostics. Coordin Chem Rev. 2021:446. doi:10.1016/j.ccr.2021.214110
  • Calzado-Martin A, Encinar M, Tamayo J, Calleja M, San Paulo A. Effect of actin organization on the stiffness of living breast cancer cells revealed by peak-force modulation atomic force microscopy. ACS Nano. 2016;10(3):3365–3374. doi:10.1021/acsnano.5b07162
  • Handel C, Schmidt BUS, Schiller J, et al. Cell membrane softening in human breast and cervical cancer cells. New J Phys. 2015:17. doi:10.1088/1367-2630/17/8/083008
  • Malohlava J, Tomankova K, Malina L, et al. Effect of porphyrin sensitizer MgTPPS4 on cytoskeletal system of hela cell line-microscopic study. Cell Biochem Biophys. 2016;74(3):419–425. doi:10.1007/s12013-016-0746-5
  • Pi J, Cai HH, Jin H, et al. Qualitative and quantitative analysis of ROS-mediated oridonin-induced oesophageal cancer KYSE-150 cell apoptosis by atomic force microscopy. PLoS One. 2015;10:10. doi:10.1371/journal.pone.0140935
  • Misiak P, Niemirowicz-Laskowska K, Markiewicz KH, et al. Evaluation of cytotoxic effect of cholesterol End-capped Poly(N-isopropylacrylamide)s on selected normal and neoplastic cells. Int J Nanomed. 2020;15:7263–7278. doi:10.2147/Ijn.S262582
  • Maja M, Mohammed D, Dumitru AC, et al. Surface cholesterol-enriched domains specifically promote invasion of breast cancer cell lines by controlling invadopodia and extracellular matrix degradation. Cell Mol Life Sci. 2022;79(8):417. doi:10.1007/s00018-022-04426-8
  • Ma X, Bi E, Lu Y, et al. Cholesterol induces CD8(+) T cell exhaustion in the tumor microenvironment. Cell Metab. 2019;30(1):143–56e5. doi:10.1016/j.cmet.2019.04.002
  • Greenlee JD, Subramanian T, Liu K, King MR. Rafting down the metastatic cascade: the role of lipid rafts in cancer metastasis, cell death, and clinical outcomes. Cancer Res. 2021;81(1):5–17. doi:10.1158/0008-5472.CAN-20-2199
  • Zhang L, Xu B, Wang X. Cholesterol extraction from cell membrane by graphene nanosheets: a computational study. J Phys Chem B. 2016;120(5):957–964. doi:10.1021/acs.jpcb.5b10330
  • Gu ZL, Yang ZX, Luan BQ, et al. Membrane insertion and phospholipids extraction by graphyne nanosheets. J Phys Chem C. 2017;121(4):2444–2450. doi:10.1021/acs.jpcc.6b10548
  • Taninaka A, Ugajin S, Kurokawa H, et al. Direct analysis of the actin-filament formation effect in photodynamic therapy. RSC Adv. 2022;12(10):5878–5889. doi:10.1039/d1ra09291j
  • Basu R, Whitlock BM, Husson J, et al. Cytotoxic T cells use mechanical force to potentiate target cell killing. Cell. 2016;165(1):100–110. doi:10.1016/j.cell.2016.01.021
  • Rudzka DA, Spennati G, McGarry DJ, et al. Migration through physical constraints is enabled by MAPK-induced cell softening via actin cytoskeleton re-organization. J Cell Sci. 2019;132(11). doi:10.1242/jcs.224071
  • Kammertoens T, Friese C, Arina A, et al. Tumour ischaemia by interferon-gamma resembles physiological blood vessel regression. Nature. 2017;545(7652):98–102. doi:10.1038/nature22311
  • Zhang XL, Li HY, Yi C, et al. Host immune response triggered by graphene quantum-dot-mediated photodynamic therapy for oral squamous cell carcinoma. Int J Nanomed. 2020;15:9627–9638. doi:10.2147/Ijn.S276153
  • Wang YQ, Zhao ZL, Liu CL, et al. B16 membrane-coated vesicles for combined photodynamic therapy and immunotherapy shift immune microenvironment of melanoma. Int J Nanomed. 2022;17:855–868. doi:10.2147/Ijn.S338488
  • Ou W, Jiang L, Thapa RK, et al. Combination of NIR therapy and regulatory T cell modulation using layer-by-layer hybrid nanoparticles for effective cancer photoimmunotherapy. Theranostics. 2018;8(17):4574–4590. doi:10.7150/thno.26758
  • Byfield FJ, Aranda-Espinoza H, Romanenko VG, Rothblat GH, Levitan I. Cholesterol depletion increases membrane stiffness of aortic endothelial cells. Biophys J. 2004;87(5):3336–3343. doi:10.1529/biophysj.104.040634
  • Khatibzadeh N, Gupta S, Farrell B, Brownell WE, Anvari B. Effects of cholesterol on nano-mechanical properties of the living cell plasma membrane. Soft Matter. 2012;8(32):8350–8360. doi:10.1039/C2SM25263E